Granulocyte colony-stimulating factor enhances bone marrow stem cell damage caused by repeated administration of cytotoxic agents.
Abstract
Despite the increasing use of cytokines to circumvent the acute dose-limiting myelotoxicity of cancer treatment, little is known about the combined effects of cytotoxic agents and cytokines on the primitive stem cells responsible for long-term hematopoiesis. In an experimental model, we administered cytotoxic agents that have variable effects on primitive stem cells in C57BL/6 (B6)-mice. Mice received six every-other-week doses of cyclophosphamide (CY, 84 mg/kg), VP-16 (24 mg/kg) + cisplatinum (2.4 mg/kg), carboplatinum (50 mg/kg), chlorambucil (12 mg/kg), BCNU (13.2 mg/kg), or TBI (80 cGy). Granulocyte colony-stimulating factor (G-CSF; 250 microg/kg/day) was administered subcutaneously twice daily on days 3 to 6 after each dose of the cytotoxic agent. Comparison with animals receiving the cytotoxic agent alone was made to investigate the effects of G-CSF on long-term hematopoiesis. Hematopoiesis was measured 20 weeks after the last dose of the cytotoxic agent by assessment of peripheral blood counts, marrow cellularity, progenitor cell content (colony-forming units-spleen; CFU-S), and primitive stem cell number (long-term repopulating ability and day 28 and day 35 cobblestone area-forming cell [CAFC] frequencies). Exposure to cytotoxic agents alone resulted in a significant decrease in primitive stem cells (as measured by repopulating units [RU] and day 28 and day 35 CAFC content) in animals given carboplatinum, chlorambucil, BCNU, and TBI, but not in animals treated with cyclophosphamide or VP-16 and cisplatinum. The addition of G-CSF resulted in a significant decrease in stem cell content when compared with no G-CSF administration in animals treated with chlorambucil, BCNU, or TBI. Thus, G-CSF administered after repeated exposure to cytotoxic agents, appeared to damage the primitive stem cell compartment when used in combination with agents known to damage primitive stem cells. These results, although obtained in an experimental model, should raise concerns for the indiscriminate use of G-CSF in the clinic.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Some irradiated patients develop long-term or residual BM injuries manifested by decreases in HSC reserves and impairments in HSC self-renewal after recovering from IR-induced acute myelosuppression.
“However, some irradiated patients also develop long-term or residual BM injuries manifested by decreases in HSC reserves and impairments in HSC self-renewal after recovering from IR-induced acute myelosuppression.”
From Total body irradiation causes long-term mouse BM injury via induction of HSC premature senescence in an Ink4a- and Arf-independent manner (2014) · cites this paper as [5]
Residual BM damage is latent, long lasting, shows little tendency for recovery, and can lead to hypoplastic anemia or myelodysplastic syndrome at a later time or after additional hematopoietic stress.
“Although residual BM damage is latent, it is long lasting, shows little tendency for recovery, and can lead to the development of hypoplastic anemia or a myelodysplastic syndrome at a later time or after additional hematopoietic stress.4,5”
From Total body irradiation causes long-term mouse BM injury via induction of HSC premature senescence in an Ink4a- and Arf-independent manner (2014) · cites this paper as [5]
Cites
The limited in vitro lifetime of human diploid cell strains
Hayflick, L. (1965) · Experimental Cell Research · doi:10.1016/0014-4827(65)90211-9 · Cited by 5,876 · see citing works
Crawford, J., Ozer, H., Stoller, R. G., Johnson, D. H., Lyman, G. H., Tabbara, I. A., Kris, M. G., Grous, J. J., Picozzi, V. J., Rausch, G., et al. (1991) · New England Journal of Medicine · doi:10.1056/nejm199107183250305 · Cited by 1,388 · see citing works
Brandt, S. J., Peters, W. P., Atwater, S. K., Kurtzberg, J., Borowitz, M. J., Jones, R. B., Shpall, E. J., Bast, R. C., Gilbert, C. J., & Oette, D. H. (1988) · New England Journal of Medicine · doi:10.1056/nejm198804073181401 · Cited by 753 · see citing works
Filgrastim (r-metHuG-CSF): the first 10 years
Welte, K., Gabrilove, J. L., Bronchud, M., Platzer, E., & Morstyn, G. (1996) · Blood · doi:10.1182/blood.v88.6.1907.bloodjournal8861907 · Cited by 599 · see citing works
Hematopoietic stem cell compartment: acute and late effects of radiation therapy and chemotherapy.
Mauch, P., Constine, L., Greenberger, J., Knospe, W., Sullivan, J., Liesveld, J. L., & Deeg, H. J. (1995) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/0360-3016(94)00430-s · Cited by 507 · see citing works
The evaluation of limiting dilution assays
Groth, S. (1982) · Journal of Immunological Methods · doi:10.1016/0022-1759(82)90269-1 · Cited by 452 · see citing works
Sheridan, W. P., Wolf, M., Lusk, J. T., Layton, J. E., de Souza, L. A., Morstyn, G., Dodds, A. J., Maher, D., Green, M. D., & Fox, R. M. (1989) · The Lancet · doi:10.1016/s0140-6736(89)91552-3 · Cited by 418 · see citing works
An in vitro limiting-dilution assay of long-term repopulating hematopoietic stem cells in the mouse
Ploemacher, R., van der Sluijs, J., Voerman, J., & Brons, N. (1989) · Blood · doi:10.1182/blood.v74.8.2755.2755 · Cited by 396 · see citing works
Moore, M. A., & Warren, D. J. (1987) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.84.20.7134 · Cited by 368 · see citing works
Competitive repopulation: a new assay for long-term stem cell functional capacity
Harrison, D. (1980) · Blood · doi:10.1182/blood.v55.1.77.77 · Cited by 329 · see citing works
Siminovitch, L., Till, J. E., & McCulloch, E. A. (1964) · Journal of Cellular and Comparative Physiology · doi:10.1002/jcp.1030640104 · Cited by 277 · see citing works
Harrison, D. E., Jordan, C. T., Zhong, R. K., & Astle, C. M. (1993) · PubMed · Cited by 273 · see citing works
Ploemacher, R., der Sluijs, J. V., van Beurden, C., Baert, M., & Chan, P. (1991) · Blood · doi:10.1182/blood.v78.10.2527.2527 · Cited by 261 · see citing works
Harrison, D. E., Astle, C. M., & Delaittre, J. A. (1978) · The Journal of Experimental Medicine · doi:10.1084/jem.147.5.1526 · Cited by 228 · see citing works
Dreger, P., Kloss, M., Petersen, B., Haferlach, T., Löffler, H., Loeffler, M., & Schmitz, N. (1995) · Blood · doi:10.1182/blood.v86.10.3970.bloodjournal86103970 · Cited by 224 · see citing works
Kay, H. E. M. (1965) · The Lancet · doi:10.1016/s0140-6736(65)90763-4 · Cited by 197 · see citing works
Neben, S., Marcus, K. J., & Mauch, P. (1993) · Blood · doi:10.1182/blood.v81.7.1960.1960 · Cited by 148 · see citing works
Proliferative capacity of murine hematopoietic stem cells.
Hellman, S., Botnick, L. E., Hannon, E. C., & Vigneulle, R. M. (1978) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.75.1.490 · Cited by 148 · see citing works
Bodine, D., Seidel, N., & Orlic, D. (1996) · Blood · doi:10.1182/blood.v88.1.89.bloodjournal88189 · Cited by 128 · see citing works
Bodine, D., Seidel, N., & Orlic, D. (1996) · Blood · doi:10.1182/blood.v88.1.89.89 · Cited by 119 · see citing works
Jd, D., & Ploemacher, R. (1993) · PubMed · Cited by 108 · see citing works
Shimamura, M., Kobayashi, Y., Yuo, A., Urabe, A., Okabe, T., Komatsu, Y., Itoh, S., & Takaku, F. (1987) · Blood · doi:10.1182/blood.v69.1.353.353 · Cited by 105 · see citing works
Hornung, R., & Longo, D. (1992) · Blood · doi:10.1182/blood.v80.1.77.77 · Cited by 94 · see citing works
Hematopoietic stem cell deficit of transplanted bone marrow previously exposed to cytotoxic agents.
Neben, S., Hellmän, S., Montgomery, M., Ferrara, J. L. M., Mauch, P., & Hemman, S. (1993) · PubMed · Cited by 86 · see citing works
Andrews, R., Briddell, R., Knitter, G., Opie, T., Bronsden, M., Myerson, D., Appelbaum, F. R., & McNiece, I. (1994) · Blood · doi:10.1182/blood.v84.3.800.800 · Cited by 80 · see citing works
Differential effects of cytotoxic agents on hematopoietic progenitors.
Botnick, L. E., Hannon, E. C., Vigneulle, R. M., & Hellmän, S. (1981) · PubMed · Cited by 80 · see citing works
Multisystem stem cell failure after apparent recovery from alkylating agents.
Botnick, L. E., Hannon, E. C., & Hellmän, S. (1978) · PubMed · Cited by 77 · see citing works
Down, J. D., Boudewijn, A., van Os, R. P., Thames, H. D., & Ploemacher, R. (1995) · Blood · doi:10.1182/blood.v86.1.122.bloodjournal861122 · Cited by 72 · see citing works
Permanent loss in stem cell self renewal capacity following stress to the marrow
Mauch, P. M., Rosenblatt, M., & Hellmän, S. (1988) · Blood · doi:10.1182/blood.v72.4.1193.1193 · Cited by 68 · see citing works
Ploemacher, R., van Os, R. P., Beurden, C. A. J. V. D. L.-V., & Down, J. D. (1992) · International Journal of Radiation Biology · doi:10.1080/09553009214551251 · Cited by 67 · see citing works
Loss of hematopoietic stem cell self-renewal after bone marrow transplantation
Mauch, P. M., & Hellmän, S. (1989) · Blood · doi:10.1182/blood.v74.2.872.872 · Cited by 64 · see citing works
Neben, S., Anklesaria, P. N., Greenberger, J. S., & Mauch, P. M. (1993) · PubMed · Cited by 63 · see citing works
Freedman, A. S., Neuberg, D. S., Mauch, P., Gribben, J. G., Soiffer, R. J., Anderson, K. C., Robertson, M. J., Fisher, D. C., Schlossman, R. L., Kroon, M., et al. (1997) · Blood · doi:10.1182/blood.v90.12.4996 · Cited by 51 · see citing works
Total marrow failure induced by pegylated stem-cell factor administered before 5-fluorouracil
Molineux, G., Migdalska, A., Haley, J. E., EVANS, G. S., & Dexter, T. M. (1994) · Blood · doi:10.1182/blood.v83.12.3491.3491 · Cited by 43 · see citing works
Gardner, R. V., Lerner, C. P., Astle, C. M., & Harrison, D. E. (1993) · Cancer Chemotherapy and Pharmacology · doi:10.1007/bf00685889 · Cited by 42 · see citing works
Botnick, L. E., Hannon, E. C., & Hellmän, S. (1979) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/0360-3016(79)90785-5 · Cited by 42 · see citing works
Mauch, P., Down, J. D., WARHOL, M., & HELLMEN, S. (1988) · Transplantation · doi:10.1097/00007890-198808000-00004 · Cited by 41 · see citing works
Familial haemophagocytic lymphohistiocytosis treated with allogeneic bone marrow transplantation.
Nespoli, L., Locatelli, F., Bonetti, F., Porta, F., Zecca, M., Gibardi, A., Gambarana, D., Vitale, V., Burgio, G. R., & Severi, F. (1991) · PubMed · Cited by 41 · see citing works
Proliferative Capacity of Murine Hematopoietic Stem Cells in Vitro
Reincke, U., Hannon, E. C., Rosenblatt, M., & Hellmän, S. (1982) · Science · doi:10.1126/science.7071580 · Cited by 40 · see citing works
Down, J. D., Boudewijn, A., Dillingh, J. H., Fox, B. W., & Ploemacher, R. (1994) · British Journal of Cancer · doi:10.1038/bjc.1994.359 · Cited by 34 · see citing works
Patchen, M., MacVittie, T. J., Solberg, B. D., & Souza, L. M. (1990) · PubMed · Cited by 31 · see citing works
Harrison, D., Zsebo, K., & Astle, C. (1994) · Blood · doi:10.1182/blood.v83.11.3146.3146 · Cited by 28 · see citing works
van Os, R. P., Dawes, D., Mislow, J. M. K., Witsell, A. L., & Mauch, P. (1997) · Blood · doi:10.1182/blood.v89.7.2376 · Cited by 28 · see citing works
Behavior of feline hematopoietic stem cells years after busulfan exposure
Abkowitz, J., Linenberger, M., Persik, M. T., Newton, M. A., & Guttorp, P. M. (1993) · Blood · doi:10.1182/blood.v82.7.2096.2096 · Cited by 27 · see citing works
Compromising Effect of Low Dose-rate Total Body Irradiation on Allogeneic Bone Marrow Engraftment
van Os, R. P., Konings, A. W. T., & Down, J. (1993) · International Journal of Radiation Biology · doi:10.1080/09553009314552011 · Cited by 20 · see citing works
van der Wall, E., Koning, C. C. E., van Zandwijk, N., Baars, J. W., Schornagel, J. H., Richel, D. J., Rutgers, E. J. T., Borger, J. H., Beijnen, J. H., & Rodenhuis, S. (1996) · European Journal of Cancer · doi:10.1016/0959-8049(96)00129-3 · Cited by 18 · see citing works
MacMillan, J. R., & Ns, W. (1982) · PubMed · Cited by 15 · see citing works
Down, J. D., de Haan, G., Dillingh, J. H., Dontje, B., & NIJHOF, W. (1997) · Radiation Research · doi:10.2307/3579480 · Cited by 9 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Bergh, J. C. S., Wiklund, T. A., Erikstein, B., Lidbrink, E. K., Lindman, H., Malmström, P., Kellokumpu‐Lehtinen, P., Bengtsson, N., Söderlund, G., Anker, G. B., et al. (2000) · The Lancet · doi:10.1016/s0140-6736(00)02841-5 · Cited by 338 · see citing works
Hematopoietic Stem Cell Injury Induced by Ionizing Radiation
Shao, L., Luo, Y., & Zhou, D. (2013) · Antioxidants and Redox Signaling · doi:10.1089/ars.2013.5635 · Cited by 337 · see citing works
Therapeutic targeting of a stem cell niche
Adams, G. B., Martin, R. P., Alley, I. R., Chabner, K. T., Cohen, K. S., Calvi, L. M., Kronenberg, H. M., & Scadden, D. T. (2007) · Nature Biotechnology · doi:10.1038/nbt1281 · Cited by 288 · see citing works
Wang, Y., Liu, L., Pazhanisamy, S. K., Li, H., Meng, A., & Zhou, D. (2010) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2009.11.005 · Cited by 273 · see citing works
Wang, Y., Probin, V., & Zhou, D. (2006) · Current Cancer Therapy Reviews · doi:10.2174/157339406777934717 · Cited by 214 · see citing works
Wright, D. E., Cheshier, S. H., Wagers, A. J., Randall, T. D., Christensen, J. L., & Weissman, I. L. (2001) · Blood · doi:10.1182/blood.v97.8.2278 · Cited by 208 · see citing works
Zhang, H., Zhai, Z., Wang, Y., Zhang, J., Wu, H., Wang, Y., Li, C., Li, D., Lu, L., Wang, X., et al. (2012) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2012.10.530 · Cited by 207 · see citing works
Shao, L., Feng, W., Li, H., Gardner, D., Luo, Y., Wang, Y., Liu, L., Meng, A., Sharpless, N. E., & Zhou, D. (2014) · Blood · doi:10.1182/blood-2013-07-515619 · Cited by 165 · see citing works
Chong, P. P., Selvaratnam, L., Abbas, A. A., & Kamarul, T. (2011) · Journal of Orthopaedic Research® · doi:10.1002/jor.21556 · Cited by 153 · see citing works
Impaired hematopoietic stem cell functioning after serial transplantation and during normal aging
Kamminga, L. M., van Os, R., Ausema, A., Noach, E. J. K., Weersing, E., Dontje, B., Vellenga, E., & de Haan, G. (2005) · STEM CELLS · doi:10.1634/stemcells.2004-0066 · Cited by 128 · see citing works
Metformin ameliorates ionizing irradiation-induced long-term hematopoietic stem cell injury in mice
Xu, G., Wu, H., Zhang, J., Li, D., Wang, Y., Wang, Y., Zhang, H., Lu, L., Li, C., Huang, S. M., et al. (2015) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2015.05.045 · Cited by 127 · see citing works
Granulocyte Colony–Stimulating Factor Administration: Adverse Events
D’Souza, A., Jaiyesimi, I. A., Trainor, L., & Venuturumilli, P. (2008) · Transfusion Medicine Reviews · doi:10.1016/j.tmrv.2008.05.005 · Cited by 114 · see citing works
Brunner, S., Winogradow, J., Huber, B. C., Zaruba, M., Fischer, R., David, R., Assmann, G., Herbach, N., Wanke, R., Mueller‐Hoecker, J., et al. (2008) · The FASEB Journal · doi:10.1096/fj.08-109462 · Cited by 90 · see citing works
Breitfeld, P. P., Lyden, E. R., Raney, R. B., Teot, L. A., Wharam, M. D., Lobe, T. E., Crist, W., Maurer, H. M., Donaldson, S. S., & Ruymann, F. B. (2001) · The American journal of pediatric hematology/oncology · doi:10.1097/00043426-200105000-00010 · Cited by 90 · see citing works
Drouet, M., Mourcin, F., Grenier, N., Leroux, V., Denis, J., Mayol, J.-F., Thullier, P., Lataillade, J., & Hérodin, F. (2003) · Blood · doi:10.1182/blood-2003-05-1400 · Cited by 81 · see citing works
Hematopoietic stem cell senescence and cancer therapy-induced long-term bone marrow injury.
Shao, L., Wang, Y., Chang, J., Luo, Y., Meng, A., & Zhou, D. (2013) · PubMed · doi:10.3978/j.issn.2218-676x.2013.07.03 · Cited by 79 · see citing works
Griscelli, A. B., Touriño, C., Izac, B., Vainchenker, W., & Coulombel, L. (1999) · Blood · doi:10.1182/blood.v94.2.529 · Cited by 80 · see citing works
Nurgalieva, Z. Z., Liu, C.-C., & Du, X. L. (2010) · Medical Oncology · doi:10.1007/s12032-010-9512-5 · Cited by 78 · see citing works
Chemotherapy-induced thrombocytopenia: literature review
Gao, A., Zhang, L., & Zhong, D. (2023) · Discover Oncology · doi:10.1007/s12672-023-00616-3 · Cited by 77 · see citing works
Brunner, S., Zaruba, M., Huber, B., David, R., Vallaster, M., Assmann, G., Mueller‐Hoecker, J., & Franz, W. (2008) · Experimental Hematology · doi:10.1016/j.exphem.2008.03.014 · Cited by 70 · see citing works
Li, H., Wang, Y., Pazhanisamy, S. K., Shao, L., Batinic-Haberle, I., Meng, A., & Zhou, D. (2011) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2011.04.016 · Cited by 68 · see citing works
Wang, Y., Liu, L., & Zhou, D. (2011) · Radiation Research · doi:10.1667/rr2727.1 · Cited by 67 · see citing works
Xiao, H., Xiong, L., Song, X., Jin, P., Chen, L., Chen, X., Yao, H., Wang, Y., & Wang, L. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18112265 · Cited by 64 · see citing works
van Os, R., Robinson, S., Sheridan, T., & Mauch, P. M. (2000) · Stem Cells · doi:10.1634/stemcells.18-2-120 · Cited by 57 · see citing works
Self-citationGranulocyte colony-stimulating factor exacerbates hematopoietic stem cell injury after irradiation
Li, C., Lu, L., Zhang, J., Huang, S. M., Xing, Y., Zhao, M., Zhou, D., Li, D., & Meng, A. (2015) · Cell & Bioscience · doi:10.1186/s13578-015-0057-3 · Cited by 55 · see citing works
Brunner, S., Huber, B. C., Fischer, R., Groebner, M., Hacker, M., David, R., Zaruba, M., Vallaster, M., Rischpler, C., Wilke, A., et al. (2008) · Experimental Hematology · doi:10.1016/j.exphem.2008.01.011 · Cited by 50 · see citing works
Papaldo, P., Ferretti, G., Cosimo, S. D., Giannarelli, D., Marolla, P., Lopez, M., Cortesi, E., Antimi, M., Terzoli, E., Carlini, P., et al. (2006) · Journal of Clinical Oncology · doi:10.1200/jco.2005.02.9488 · Cited by 42 · see citing works
Zhang, J., Xue, X., Han, X., Li, Y., Lu, L., Li, D., & Fan, S. (2017) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2017/8241678 · Cited by 34 · see citing works
Robinson, S. N., Freedman, A. S., Neuberg, D. S., Nadler, L. M., & Mauch, P. (2000) · Experimental Hematology · doi:10.1016/s0301-472x(00)00547-6 · Cited by 31 · see citing works
Sca+CD34− murine side population cells are highly enriched for primitive stem cells
Parmar, K., Sauk-Schubert, C., Burdick, D., Handley, M., & Mauch, P. (2003) · Experimental Hematology · doi:10.1016/s0301-472x(02)01074-3 · Cited by 30 · see citing works
Gilleece, M. H., Pearce, R., Linch, D. C., Wilson, M. C., Towlson, K. E., Mackinnon, S., Potter, M. N., Kazmi, M. A., Gribben, J. G., & Marks, D. I. (2008) · Hematology · doi:10.1179/102453308x315915 · Cited by 29 · see citing works
Vantelon, J., Koscielny, S., Brault, P., Bourhis, J. H., Ribrag, V., Pico, J., Fenaux, P., & Munck, J. (2000) · Bone Marrow Transplantation · doi:10.1038/sj.bmt.1702201 · Cited by 28 · see citing works
Chemotherapy prior to autologous bone marrow transplantation impairs long-term engraftment in mice
Noach, E. J. K., Ausema, A., van Os, R. P., Akkerman, I., Koopal, S., Weersing, E., Dontje, B., Vellenga, E., & de Haan, G. (2003) · Experimental Hematology · doi:10.1016/s0301-472x(03)00068-7 · Cited by 25 · see citing works
Thioredoxin mitigates radiation-induced hematopoietic stem cell injury in mice
Sundaramoorthy, P., Wang, Q., Zheng, Z., Jiao, Y., Chen, B. J., Doan, P. L., Chao, N. J. A., & Kang, Y. (2017) · Stem Cell Research & Therapy · doi:10.1186/s13287-017-0711-2 · Cited by 24 · see citing works
Zhang, J., Li, H., Lu, L., Yan, L., Yang, X., Shi, Z., & Li, D. (2016) · Journal of Radiation Research · doi:10.1093/jrr/rrw056 · Cited by 21 · see citing works
Gardner, R. V., Begue, R., & McKinnon, E. (2001) · Experimental Hematology · doi:10.1016/s0301-472x(01)00685-3 · Cited by 20 · see citing works
Goff, B. A., Mandel, L. S., Muntz, H. G., & Melancon, C. H. (2000) · Cancer · doi:10.1002/1097-0142(20001115)89:10 · Cited by 505 · see citing works
Cairns, J., Leonard, E., Khan, K., Parks, C., Maglennon, G. A., Zhang, B., Lazic, S. E., Ewart, L. C., & David, R. M. (2023) · Frontiers in Pharmacology · doi:10.3389/fphar.2023.1142581 · Cited by 16 · see citing works
rhTPO Ameliorates Radiation-Induced Long-Term Hematopoietic Stem Cell Injury in Mice
Luan, H., Yang, J., Wang, Y., Shen, X., Zhang, X., Qiao, Z., Xing, S. J., & Yu, Z.-Y. (2023) · Molecules · doi:10.3390/molecules28041953 · Cited by 13 · see citing works
Qian, L., Xiang, D., Zhang, J., Zhu, S., Gao, J., Wang, X., Gao, J., Zhang, Y., Shen, J., Yu, Y., et al. (2012) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2012.11.002 · Cited by 13 · see citing works
Analysis of the stem cell sparing properties of cyclophosphamide
Gardner, R. V., McKinnon, E., & Astle, C. M. (2001) · European Journal Of Haematology · doi:10.1034/j.1600-0609.2001.067001014.x · Cited by 13 · see citing works
Takeyama, K. (2003) · Japanese Journal of Clinical Oncology · doi:10.1093/jjco/hyg013 · Cited by 12 · see citing works
Brunner, S., Huber, B. C., Weinberger, T., Vallaster, M., Wollenweber, T., Gerbitz, A., Hacker, M., & Franz, W. (2011) · Journal of Cellular and Molecular Medicine · doi:10.1111/j.1582-4934.2011.01286.x · Cited by 10 · see citing works
Noach, E. J. K., Ausema, A., Dillingh, J. H., Dontje, B., Weersing, E., Akkerman, I., Vellenga, E., & de Haan, G. (2002) · Blood · doi:10.1182/blood.v100.1.312 · Cited by 9 · see citing works
Araki, D., Chen, V., Redekar, N. R., Salisbury-Ruf, C. T., Luo, Y., Liu, P., Li, Y., Smith, R. H., Dagur, P. K., Combs, C. A., et al. (2024) · Cell stem cell · doi:10.1016/j.stem.2024.10.013 · Cited by 10 · see citing works
Özbek, N. Y., Yetgin, S., & Tuncer, A. M. (2000) · Leukemia Research · doi:10.1016/s0145-2126(99)00138-1 · Cited by 8 · see citing works
Latent hematopoietic stem cell toxicity associated with protracted drug administration
Keyes, K. A., Segovia, J. C., Bueren, J. A., Parchment, R. E., & Albella, B. (2001) · Experimental Hematology · doi:10.1016/s0301-472x(00)00670-6 · Cited by 8 · see citing works
Molyneux, G., Rizzo, S., Gibson, F. M., Sulsh, S., Andrews, C. M., Pilling, A. M., Nakshbandi, T., Gordon‐Smith, E. C., & Turton, J. A. (2004) · Comparative Clinical Pathology · doi:10.1007/s00580-004-0524-4 · Cited by 7 · see citing works
Sitagliptin Mitigates Total Body Irradiation-Induced Hematopoietic Injury in Mice
Wang, M., Dong, Y., Wu, J., Li, H., Zhang, J., Lu, L., Zhang, Y., Zhou, Z., Fan, S., Li, D., et al. (2020) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2020/8308616 · Cited by 6 · see citing works
IEPA, a novel radiation countermeasure, alleviates acute radiation syndrome in rodents
Wesołowski, R., Fish, B. L., Eibl, M., Bähr, S., Mehta, S. M., Czajkowski, M. T., Gasperetti, T., Orschell, C. M., Asang, C., Singh, N., et al. (2024) · International Journal of Radiation Biology · doi:10.1080/09553002.2024.2425312 · Cited by 5 · see citing works
Modulatory Effect of Dopamine on Doxorubicin-induced Myelosuppression
Ray, M. R., Lakshmi, C. N., Deb, C., Ray, C. M. P., & Lahiri, T. (2001) · Comparative Clinical Pathology · doi:10.1007/s005800170008 · Cited by 5 · see citing works
Kim, Y., Jeong, J., Park, K., Sohn, K., Yoon, S. Y., & Kim, J. W. (2021) · Radiation Research · doi:10.1667/rade-20-00288.1 · Cited by 5 · see citing works
Plett, P. A., Chua, H. L., Wu, T., Sampson, C. H., Guise, T. A., Wright, L. E., Pagnotti, G. M., Feng, H., Chin-Sinex, H., Pike, F., et al. (2024) · Radiation Research · doi:10.1667/rade-24-00065.1 · Cited by 4 · see citing works
Liesveld, J. L., Rubin, P., & Constine, L. S. (2013) · Medical radiology · doi:10.1007/978-3-540-75863-1_24 · Cited by 4 · see citing works
Turner, S. D., Rafferty, J. A., Fairbairn, L., Ashby, J., Tinwell, H., Eckert, H.-G., Baum, C., & Lashford, L. S. (2000) · Leukemia · doi:10.1038/sj.leu.2401810 · Cited by 4 · see citing works
Thrombocytosis in cancer patients: when more is not better—in fact, the opposite
Aleksandrowicz, K., Polityńska, B., Kruszewska, J., Radziwon, P., Wojtukiewicz, A. M., Honn, K. V., & Wojtukiewicz, M. Z. (2026) · Cancer and Metastasis Reviews · doi:10.1007/s10555-025-10309-8 · Cited by 3 · see citing works
Kim, M., Moon, W., Heo, J., Lim, S., Lee, S., Jeong, J., & Lee, S. J. (2022) · World Journal of Stem Cells · doi:10.4252/wjsc.v14.i3.245 · Cited by 4 · see citing works
Murine Side Population Cells Contain Cobblestone Area-forming Cell Activity in Mobilized Blood
Parmar, K., Burdick, D., Ethier, M., Clyne, J., & Mauch, P. (2005) · Stem Cells and Development · doi:10.1089/scd.2005.14.452 · Cited by 3 · see citing works
Su, L., Dong, Y., Guan, B., Wang, Y., Lu, Y., Wang, X., Li, W., Huo, Q., Meng, A., & Li, D. (2025) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2025.1544320 · Cited by 1 · see citing works
Veeraperumal, S., Gawali, B., Singh, N., Sevim-Wunderlich, S., Czajkowski, M. T., Mehta, S. M., Asang, C., Pleimes, D., & Pawar, S. A. (2025) · International Journal of Radiation Biology · doi:10.1080/09553002.2025.2505526 · Cited by 1 · see citing works
Zhang, Y., Liu, Y., Xu, J., Zhang, Q., Zhu, X., Peng, J., Feng, G., Peng, J., Hou, M., Shao, L., et al. (2026) · Frontiers in Medicine · doi:10.3389/fmed.2026.1898479 · Cited by 1 · see citing works
Yang, W., Chen, C., Jiang, X., Zhao, Y., Wang, J., Zhang, Q., Zhang, J., Feng, Y., & Cui, S. (2024) · Cell Biology International · doi:10.1002/cbin.12140 · Cited by 1 · see citing works
Thrombocytopenia in solid malignancies: A review
Sharma, D., & Sharma, N. (2022) · IP International Journal of Medical Paediatrics and Oncology · doi:10.18231/j.ijmpo.2022.024
Xu, W., Han, H., Li, B., Huang, R., Qing, L., & Zhang, G. (2025) · Blood Cells Molecules and Diseases · doi:10.1016/j.bcmd.2025.102965
- Authors
- van Os, R., Robinson, S., Sheridan, T., Mislow, J. M. K., Dawes, D., & Mauch, P. M.
- Affiliations
- From the Joint Center for Radiation Therapy, Department of Radiation Oncology, Harvard Medical School, Boston, MA.
- Harvard University (US)
- ORCID
- Mauch, Peter M.
- Venue
- Blood
- Publisher
- American Society of Hematology
- Published
- 1998-09-15
- Volume
- 92
- Issue
- 6
- Pages
- 1950-1956
- ISSN
- 0006-4971 (ISSN-L)
- 1528-0020
- OpenAlex
- W142692312
- Cited by
- 64
- References
- 47
- Citations by year
- 2026: 2 · 2025: 3 · 2024: 4 · 2023: 3 · 2022: 2 · 2021: 1 · 2020: 1 · 2017: 3 · 2016: 1 · 2015: 2 · 2014: 1 · 2013: 3 · 2012: 2
- FWCI
- 2.79
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Blood (publishedVersion)
- PubMed (publishedVersion)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (publishedVersion)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion)
- Funders
- Centers for Disease Control and Prevention (P50 HK54785-01)
- National Cancer Institute (R01CA010941, R01-CA10941-26)
- Topics
- Health Sciences › Medicine › Hematology › Hematopoietic Stem Cell Transplantation
- Health Sciences › Medicine › Oncology › Neutropenia and Cancer Infections
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Blood disorders and treatments
- Keywords
- granulocyte colony-stimulating factor, bone marrow-derived stem cells, myelosuppression, long-term hematopoiesis, cobblestone area-forming cells, CFU-S, cyclophosphamide, carboplatin, chlorambucil, BCNU, total body irradiation, hematopoietic progenitor cells, cytokine therapy
- MeSH terms
- Animals, Antineoplastic Combined Chemotherapy Protocols, Bone Marrow Cells, Cell Count, Cyclophosphamide, Drug Administration Schedule, Etoposide, Male, Mice, Inbred C57BL, Stem Cells, Granulocyte Colony-Stimulating Factor, Mice
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
